The Role of Grasslands in a Green Future 3 Potential of legume-based grassland-livestock systems in Europe Lüscher A. 1 , Mueller-Harvey I. 2 , Soussana J.F. 3 , Rees R.M. 4 and Peyraud J.L. 5 1 Agroscope Reckenholz-Tänikon Research Station ART, 8046 Zurich, Switzerland 2 University of Reading, Reading RG6 6AT, United Kingdom 3 INRA, Grassland Ecosystem Research, 63100 Clermont-Ferrand, France 4 Scotland’s Rural College, Edinburgh EH9 3JG, United Kingdom 5 INRA, UMR PEGASE, 35590 St Gilles, France Corresponding author: [email protected]Abstract European grassland-based livestock production systems are challenged to produce more milk and meat to meet increasing world demand and to achieve this by using fewer resources. Legumes offer great potential for coping with such requests. They have numerous features that can act together at different stages in the soil-plant-animal-atmosphere system and these are most effective in mixed swards with a legume abundance of 30-50%. The resulting benefits are a reduced dependency on fossil energy and industrial N fertilizer, lower quantities of harmful emissions to the environment (greenhouse gases and nitrate), lower production costs, higher productivity and increased protein self-sufficiency. Some legume species offer opportunities for improving animal health with less medication due to bioactive secondary metabolites. In addition, legumes may offer an option for adapting to higher atmospheric CO 2 concentrations and to climate change. Legumes generate these benefits at the level of the managed land area unit and also at the level of the final product unit. However, legumes suffer from some limitations, and suggestions are made for future research in order to exploit more fully the opportunities that legumes can offer. In conclusion, the development of legume-based grassland-livestock systems undoubtedly constitutes one of the pillars for more sustainable and competitive ruminant production systems, and it can only be expected that legumes will become more important in the future. Keywords: yield, symbiotic N 2 fixation, forage quality, nutritive value, voluntary intake, animal performance, greenhouse gas emission, nitrate leaching, condensed tannins, animal health, clover, climate change, energy, plant secondary metabolites, management Introduction European grassland-based livestock production systems have changed considerably over the last two decades and will continue to evolve in response to societal and environmental pressures. Grassland production will need to keep pace with requirements for higher meat and milk production from ruminant systems and with a changing climate. At the same time, grassland production needs to minimize competition from arable land and between food and feed production, and preserve biodiversity and ecosystem services (Thornton, 2010). Legumes offer important opportunities for sustainable grassland-based animal production because they can contribute to important key challenges by (i) increasing forage yield, (ii) substituting inorganic N fertilizer inputs with symbiotic N 2 fixation, (iii) mitigating and supporting adaptation to climate change, as elevated atmospheric CO 2 , warmer temperatures and drought-stress periods increase, and (iv) increasing the nutritive value of herbage and raising the efficiency of conversion of herbage to animal protein. A concerted programme of research supported by the European Commission is devoted to improving our understanding of the roles played by legumes in grassland systems. Of
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The Role of Grasslands in a Green Future 3
Potential of legume-based grassland-livestock systems in Europe
Lüscher A.
1, Mueller-Harvey I.
2, Soussana J.F.
3, Rees R.M.
4 and Peyraud J.L.
5
1 Agroscope Reckenholz-Tänikon Research Station ART, 8046 Zurich, Switzerland
2 University of Reading, Reading RG6 6AT, United Kingdom
3 INRA, Grassland Ecosystem Research, 63100 Clermont-Ferrand, France
4 Scotland’s Rural College, Edinburgh EH9 3JG, United Kingdom
Basset-Mens C., Ledgard S. and Boyes M. (2009) Eco-efficiency of intensification scenarios for milk production
in New Zealand. Ecological Economics 68, 1615-1625.
Beever D.E. and Siddons R.C. (1984) Digestion and metabolism in the grazing ruminant. In: Milligan L.P.,
Grovum W.L. and Dobson A. (eds) Control of Digestion and Metabolism in Ruminants. Proceedings of the 6th
International Symposium on Ruminant Physiology, Banff (Canada), Prentice-Hall, Englewood Cliffs, N.J.
(USA), pp. 479-497.
Beever D.E., Dhanoa M.S., Losada H.R., Evans R.T., Cammell S.B. and France J. (1986) The effect of forage
species and stage of harvest on the process of digestion occurring in the rumen of cattle. British Journal of
Nutrition 56, 439-454.
Besnard A., Montarges-Lellahi A. and Hardy A. (2006) Système de culture et nutrition azotée. Effets sur les
émissions de GES et le bilan énergétique. Fourrages 187, 311-320.
Boller B., Schubiger F.X. and Kölliker R. (2010) Red clover. In: Boller B., Posselt U.K. and Veronesi F. (eds)
Fodder Crops and Amenity Grasses, Handbook of plant breeding, Vol 5. Springer, New York, USA, pp. 439-
456.
Boller B.C. and Nösberger J. (1987) Symbiotically fixed nitrogen from field-grown white and redclover mixed
with ryegrasses at lowlevels of 15N-fertilization. Plant and Soil 104, 219-226.
Bowman W. D., Schardt J. C. and Schmidt S. K. (1996) Symbiotic N2-fixation in alpine tundra: ecosystem input
and variation in fixation rates among communities. Oecologia, 108, 345-350.
Brito A.F., Tremblay G.F., Bertrand A., Castonguay Y., Bélanger G., Michaud R., Lapierre H., Benchaar C.,
Petit H.V., Ouellet D.R. and Berthiaume R. (2008) Alfalfa cut at sundown and harvested as baleage improves
milk yield of late-lactation dairy cows. Journal of Dairy Science 91, 3968-3982.
Brown L., Scholefield D., Jewkes E.C., Preedy N., Wadge K. and Butler M. (2000) The effect of sulphur
application on the efficiency of nitrogen use in two contrasting grassland soils. The Journal of Agricultural
Science 135 131-138.
The Role of Grasslands in a Green Future 21
Burke J.M., Miller J.E., Mosjidis J.A. and Terrill T.H. (2012) Grazing sericea lespedeza for control of gastrointestinal nematodes in lambs. Veterinary Parasitology 186, 507-512. Campbell B.C., Stafford Smith D.M., Ash A.J., Fuhrer J., Gifford R.M., Hiernaux P., Howden S.M., Jones M.B., Ludwig J.A., Manderscheid R., Morgan J.A., Newton P.C.D., Nösberger J., Owensby C.E., Soussana J.F., Tuba Z. and ZuoZhong C. (2000) A synthesis of recent global change research on pasture and rangeland production: reduced uncertainties and their management implications. Agriculture, Ecosystems and Environment 82, 39-55. Cardinale B.J., Wright J.P., Cadotte M.W., Carroll I.T., Hector A., Srivastava D.S., Loreau M. and Weis J.J. (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proceedings of the National Academy of Sciences of the United States of America 104, 18123-18128. Carlsson G. and Huss-Danell K. (2003) Nitrogen fixation in perennial forage legumes in the field. Plant and Soil 253, 353-372. Carlsson G., Palmborg C., Jumpponen A., Scherer-Lorenzen M., Högberg P. and Huss-Danell K. (2009) N2 fixation in three perennial Trifolium species in experimental grasslands of varied plant species richness and composition. Plant Ecology 205, 87-104. Castle M.E., Reid D. and Watson J.N. (1983) Silage and milk production: studies with diets containing white clover silage. Grass and Forage Science 38, 193-200. Chenais F. (1993) Ensilage de légumineuses et production laitière. Fourrages 134, 258-265. Christopher S.F. and Lal R. (2007) Nitrogen management affects carbon sequestration in North American cropland soils. Critical Reviews in Plant Sciences 26, 45-64. Cohen D.C., Stockdale C.R. and Doyle P.T. (2006) Feeding an energy supplement with white clover silage improves rumen fermentation, metabolisable protein utilisation and milk production in dairy cows. Australian
Journal of Agricultural Research 57, 367-375. Connolly J., Bell T., Bolger T., Brophy C., Carnus T., Finn J.A., Kirwan L., Isbell F., Levine J., Lüscher A., Picasso V., Roscher C., Sebastia M.T., Suter M. and Weigelt A. (2013) An improved model to predict the effects of changing biodiversity levels on ecosystem function. Journal of Ecology 101, 344-355. Cralle H.T. and Heichel G.H. (1982) Temperature and chilling sensitivity of nodule nitrogenase activity in unhardened alfalfa. Crop Science 22, 300-304. Daepp M., Nösberger J. and Lüscher A. (2001) Nitrogen fertilization and developmental stage alter the response of Lolium perenne to elevated CO2. New Phytologist 150, 347-358. Davies W.E. and Young N.R. (1967) The characteristics of European, Mediterranean and other populations of white clover (Trifolium repens L.). Euphytica 16, 330-340. Delaby L. and Peccatte J.R. (2003) Valeur alimentaire des prairies d’association ray grass anglais/trèfle blanc utilisées entre 6 et 12 semaines de repousse. Rencontres Recherches Ruminants 10, 389. Dewhurst R.J., Fisher W.J., Tweed J.K.S. and Wilkins R.J. (2003) Comparison of grass and legume silages for milk production. 1. Production responses with different levels of concentrate. Journal of Dairy Science 86, 2598-2611. Dewhurst R.J., Delaby L., Moloney A., Boland T. and Lewis E. (2009) Nutritive value of forage legumes used for grazing and silage. Irish Journal of Agricultural and Food Research 48, 168-187. Dixon R.A., Liu C. and Jun J.H. (2012) Metabolic engineering of anthocyanins and condensed tannins in plants. Current Opinion in Biotechnology 24, 329-335. ecoinvent Centre (2010) ecoinvent Data - The Life Cycle Inventory Data V2.2. Swiss Centre for Life Cycle Inventories, Dübendorf, Available at http://www.ecoinvent.org (accessed on 12 February 2013). Egan A.R. and Ulyatt M.J. (1980) Quantitative digestion of fresh herbage by sheep. The Journal of Agricultural
Science 94, 47-56. European Commission (2010) The CAP towards 2020: meeting the food, natural resources and territorial challenges of the future. Communication from the Commission to the European Parliament, the Council, the European Economic and Social Committee and the Committee of the Regions, Brussels, 18 November, COM(2010) 672 final. European Parliament (2011) The EU protein deficit: what solution for a long-standing problem? European Parliament, Brussels. Faurie O., Soussana J.F. and Sinoquet H. (1996) Radiation interception, partitioning and use in grass-clover mixtures. Annals of Botany 77, 35-45. Finn J.A., Kirwan L., Connolly J., Sebastià M.T., Helgadóttir Á., Baadshaug O.H., Bélanger G., Black A., Brophy C., Collins R.P., op J., Dalmannsdóttir S., Delgado I., Elgersma A., Fothergill M., Frankow-Lindberg B.E., Ghesquire A., Golinska B., Golinski P., Grieu P., Gustavsson A.M., Höglind M., Huguenin-Elie O., Jørgensen M., Kadžiulien Ž., Kurki P., Llurba R., Lunnan T., Porqueddu C., Suter M., Thumm U. and Lüscher A. (2013) Ecosystem function enhanced by combining four functional types of plant species in intensively managed grassland mixtures: a 3-year continental-scale field experiment. Journal of Applied Ecology 50, 365-375.
22 Grassland Science in Europe, Vol. 18
Frame J. (1986) The production and quality potential of four forage legumes sown alone and combined in
various associations. Crop Research 25, 103-122.
Frame J. (1991) Herbage production and quality of a range of secondary grass species at five rates of fertilizer
nitrogen application. Grass and Forage Science 46, 139-151.
Frame J. (2005) Forage Legumes for Temperate Grasslands, Food and Agriculture Organization of the United
Nations, Rome, Science Publishers Inc., Plymouth, UK, 309 pp.
Galloway J.N., Townsend A.R., Erisman J.W., Bekunda M., Cai Z.C., Freney J.R., Martinelli L.A., Seitzinger
S.P. and Sutton M.A. (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential
solutions. Science 320, 889-892.
Gately T.F. (1981) Evaluation of the role of white clover (cv Blanca) for milk production. Winter Meeting
British Grassland Society, 5.1-5.3.
Godfray H.C.J., Beddington J.R., Crute I.R., Haddad L., Lawrence D., Muir J.F., Pretty J., Robinson S., Thomas
S.M. and Toulmin C. (2010) Food security: the challenge of feeding 9 billion people. Science 327, 812-818.
Gruber N. and Galloway J.N. (2008) An earth-system perspective of the global nitrogen cycle. Nature 451, 293-
296.
Guckert A. and Hay R.K.M. (2001) The overwintering, spring growth, and yield in mixed species swards of
white clover in Europe. Annals of Botany 88, 667-668.
Häring D.A., Suter D., Amrhein N. and Lüscher A. (2007) Biomass allocation is an important determinant of
tannin concentration in growing plants. Annals of Botany 99, 111-120.
Häring D.A., Scharenberg A., Heckendorn F., Dohme F., Lüscher A., Maurer V., Suter D. and Hertzberg H. (2008) Tanniferous forage plants: agronomic performance, palatability and efficacy against parasitic nematodes
in sheep. Renewable Agriculture and Food Systems 23, 19-29.
Harris S.L., Auldist M.J., Clark D.A. and Jansen E.B.L. (1998) Effect of white clover content in the diet on
herbage intake, milk production and milk composition of New Zealand dairy cows housed indoors. Journal of
Dairy Research 65, 389-400.
Hartwig U.A. (1998) The regulation of symbiotic N2 fixation: a conceptual model of N feedback from the
ecosystem to the gene expression level. Perspectives in Plant Ecology, Evolution and Systematics 1, 92-120.
Hebeisen T., Lüscher A., Zanetti S., Fischer B.U., Hartwig U.A., Frehner M., Hendrey G.R., Blum H. and
Nösberger J. (1997) Growth response of Trifolium repens L. and Lolium perenne L. as monocultures and bi-
species mixture to free air CO2 enrichment and management. Global Change Biology 3, 149-160.
Heichel G.H. and Henjum K.I. (1991) Dinitrogen fixation, nitrogen transfer, and productivity of forage legume-grass
communities. Crop Science 31, 202-208.
Henry G.H.R. and Svoboda J. (1986) Dinitrogen fixation (acetylene reduction) in high-Arctic sedge meadow
communities. Arctic and Alpine Research 18, 181-187.
Herridge D.F., Peoples M.B. and Boddey R.M. (2008) Global inputs of biological nitrogen fixation in
agricultural systems. Plant and Soil 311, 1-18.
Hill J. (1990) The three C’s – competition, coexistence and coevolution – and their impact on the breeding of
forage crop mixtures. Theoretical and Applied Genetics 79, 168-176.
Hille Ris Lambers J., Harpole W.S., Tilman D., Knops J. and Reich P.B. (2004) Mechanisms responsible for the
positive diversity-productivity relationship in Minnesota grasslands. Ecology Letters 7, 661-668.
Hooda P.S., Moynagh M., Svoboda I.F. and Anderson H.A. (1998) A comparative study of nitrate leaching from
intensively managed monoculture grass and grass-clover pastures. The Journal of Agricultural Science 131, 267-
275.
Hooper D.U. and Dukes J.S. (2004) Overyielding among plant functional groups in a long-term experiment.
Ecology Letters 7, 95-105.
Hooper D.U. and Vitousek P.M. (1997) The effects of plant composition and diversity on ecosystem processes.
Science 277, 1302-1305.
Hooper D.U. and Vitousek P.M. (1998) Effects of plant composition and diversity on nutrient cycling.
Ecological Monographs 68, 121-149.
Hooper D.U., Chapin F.S., Ewel J.J., Hector A., Inchausti P., Lavorel S., Lawton J.H., Lodge D.M., Loreau M.,
Naeem S., Schmid B., Setälä H., Symstad A.J., Vandermeer J. and Wardle D.A. (2005) Effects of biodiversity
on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3-35.
Gamfeldt L. and O'Connor M.I. (2012) A global synthesis reveals biodiversity loss as a major driver of
ecosystem change. Nature 486, 105-108.
Hoste H., Jackson F., Athanasiadou S., Thamsborg S.M. and Hoskin S.O. (2006) The effects of tannin-rich
plants on parasitic nematodes in ruminants. Trends in Parasitology 22, 253-261.
Humphreys J., Casey I.A. and Laidlaw A.S. (2009) Comparison of milk production from clover-based and
fertilizer-N-based grassland on a clay-loam soil under moist temperate climatic conditions. Irish Journal of
Agricultural and Food Research 48, 189-207.
The Role of Grasslands in a Green Future 23
Ineson P., Coward P.A. and Hartwig U.A. (1998) Soil gas fluxes of N2O, CH4 and CO2 beneath Lolium perenne under elevated CO2: the Swiss free air carbon dioxide enrichment experiment. Plant and Soil 198, 89-95. Institut de l’Elevage (2004) Associations graminées-trèfle blanc, le pâturage gagnant. Collection Synthèses, Technipel, Paris, France, 64 p. INRA (2007) Alimentation des bovins, ovins et caprins. Besoins des animaux. Valeur des aliments. Tables INRA 2007. Editions Quae, Paris, France, 307 pp. IPCC (2006) Guidelines for National Greenhouse Gas Inventories. Intergovernmental Panel on Climate Change, Tokyo, Japan.
Jacot K.A., Lüscher A., Nösberger J. and Hartwig, U.A. (2000a) The relative contribution of symbiotic N2 fixation and other nitrogen sources to grassland ecosystems along an altitudinal gradient in the Alps. Plant and
Soil 225, 201-211. Jacot K.A., Lüscher A., Nösberger J. and Hartwig, U.A. (2000b) Symbiotic N2 fixation of various legume species along an altitudinal gradient in the Swiss Alps. Soil Biology and Biochemistry 32, 1043-1052. Jamot J. and Grenet E. (1991) Microscopic investigation of changes in histology and digestibility in the rumen of a forage grass and forage legume during the first growth stage. Reproduction, Nutrition, Développement 31, 441-450. Jarvis S.C. and Barraclough D. (1991) Variations in mineral nitrogen under grazed grassland swards. Plant and
Soil 138, 177-188. Jayanegara A., Leiber F. and Kreuzer M. (2012) Meta-analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments. Journal of Animal Physiology and
Animal Nutrition 96, 356-375. Jensen E.S., Peoples M.B., Boddey R.M., Gresshoff P.M., Hauggaard-Nielsen H., Alves B.J.R. and Morrison M.J. (2012) Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries. A review. Agronomy for Sustainable Development 32, 329-364. Jones B.A., Muck R.E. and Hatfield R.D. (1995) Red clover extracts inhibit legume proteolysis. Journal of the
Science of Food and Agriculture 67, 329-333. Jones W.T. and Mangan J.L. (1977) Complexes of the condensed tannins of sainfoin (Onobrychis viciifolia) with fraction 1 leaf protein and with submaxillary mycoprotein, and their reversal by polyethylene glycol and pH. Journal of the Science of Food and Agriculture 28, 126-136. Kaltschmitt M. and Reinhardt G.A. (1997) Nachwachsende Energieträger - Grundlagen, Verfahren, ökologische
Bilanzierung, Vieweg Verlag, Braunschweig/Wiesbaden, Germany. Kessler W., Boller B.C. and Nösberger J. (1990) Distinct influence of root and shoot temperature on nitrogen fixation by white clover. Annals of Botany 65, 341-346. Kingston-Smith A.H., Bollard A.L., Shaw R.K., Davies T.E. and Theodorou M.K. (2003) Correlations between protein content and protease activity in forage crops. Aspects of Applied Biology 70, 101-106. Kingston-Smith A.H., Edwards J.E., Huws S.A., Kim E.J. and Abberton M. (2010) Plant-based strategies towards minimising ‘livestock’s long shadow’. Proceedings of the Nutrition Society 69, 613-620. Kirkby C.A., Kirkegaard J.A., Richardson A.E., Wade L.J., Blanchard C. and Batten G. (2011) Stable soil organic matter: a comparison of CNPS ratios in Australian and other world soils. Geoderma 163, 197-208. Kirwan L., Luescher A., Sebastià M.T., Finn J.A., Collins R.P., Porqueddu C., Helgadóttir Á., Baadshaug O.H., Brophy C., Coran C., Dalmannsdóttir S., Delgado I., Elgersma A., Fothergill M., Frankow-Lindberg B.E., Golinski P., Grieu P., Gustavsson A.M., Höglind M., Huguenin-Elie O., Iliadis C., Jørgensen M., Kadžiulien Ž., Karyotis T., Lunnan T., Malengier M., Maltoni S., Meyer V., Nyfeler D., Nykanen-Kurki P., Parente J., Smit H.J., Thumm U. and Connolly J. (2007) Evenness drives consistent diversity effects in intensive grassland systems across 28 European sites. Journal of Ecology 95, 530-539. Kirwan L., Connolly J., Finn J.A., Brophy C., Lüscher A., Nyfeler D. and Sebastià M.T. (2009) Diversity-interaction modeling: estimating contributions of species identities and interactions to ecosystem function. Ecology 90, 2032-2038. Kitani O., Jungbluth T., Peath R.M., and Ramdani A. (eds., 1999) CIGR handbook of agricultural engineering. Volume V: Energy & Biomass Engineering. American Society of Agricultural Engineers, St Joseph, USA. Klumpp K., Bloor J.M.G., Ambus P. and Soussana J.F. (2011) Effects of clover density on N2O emissions and plant-soil N transfers in a fertilized upland pasture. Plant and Soil 343, 97-107. Le Gall A., Beguin E., Dollé J.B., Manneville V. and Pflimlin A. (2009) Nouveaux compromis techniques pour concilier les impératifs d’efficacité économique et environnementale en élevage herbivore. Fourrages 198, 131-152. Ledgard S.F. and Steele K.W. (1992) Biological nitrogen-fixation in mixed legume/grass pastures. Plant and
Soil 141, 137-153. Ledgard S.F., Penno J.W. and Sprosen M.S. (1999) Nitrogen inputs and losses from clover/grass pastures grazed by dairy cows, as affected by nitrogen fertilizer application. The Journal of Agricultural Science132, 215-225.
24 Grassland Science in Europe, Vol. 18
Ledgard S., Schils R., Eriksen J. and Luo J. (2009) Environmental impacts of grazed clover/grass pastures. Irish
Journal of Agricultural and Food Research 48, 209-226. Lee M.R.F., Harris L.J., Moorby J.M., Humphreys M.O., Theodorou M.K., MacRae J.C. and Scollan N.D. (2002) Rumen metabolism and nitrogen flow to the small intestine in steers offered Lolium perenne containing different levels of water-soluble carbohydrate. Animal Science 74, 587-596. Li L., Li S.M., Sun J.H., Zhou L.L., Bao X.G., Zhang H.G. and Zhang F.S. (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proceedings of
the National Academy of Sciences of the United States of America, 104, 11192-11196. Loiseau P., Carrère P., Lafarge M., Delpy R. and Dublanchet J. (2001) Effect of soil-N and urine-N on nitrate leaching under pure grass, pure clover and mixed grass/clover pastures. European Journal of Agronomy 14, 113-121. Loreau M. and Hector A. (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72-76. Loreau M., Naeem S., Inchausti P., Bengtsson J., Grime J.P., Hector A., Hooper D.U., Huston M.A., Raffaelli D., Schmid B., Tilman D. and Wardle D.A. (2001) Biodiversity and ecosystem functioning: Current knowledge and future challenges. Science 294, 804-808. Lüscher A. and Jacquard P. (1991) Coevolution between interspecific plant competitors? Trends in Ecology and
Evolution 6, 355-358. Lüscher A., Connolly J. and Jacquard P. (1992) Neighbour specificity between Lolium perenne and Trifolium
repens from a natural pasture. Oecologia 91, 404-409. Lüscher A., Hendrey G.R. and Nösberger J. (1998) Long-term responsiveness to free air CO2 enrichment of functional types, species and genotypes of plants from fertile permanent grassland. Oecologia, 113 37-45. Lüscher A., Hartwig U.A., Suter D. and Nösberger J. (2000) Direct evidence that symbiotic N2 fixation in fertile grassland is an important trait for a strong response of plants to elevated atmospheric CO2. Global Change
Biology 6, 655-662. Lüscher A., Daepp M., Blum H., Hartwig U.A. and Nösberger J. (2004) Fertile temperate grassland under elevated atmospheric CO2 – role of feed-back mechanisms and availability of growth resources. European
Journal of Agronomy 21, 379-398. Lüscher A., Fuhrer J. and Newton P.C.D. (2005) Global atmospheric change and its effect on managed grassland systems. In: McGilloway D.A. (ed) Grassland: a global resource, Wageningen Academic Publishers, Wageningen, The Netherlands, pp. 251-264. Lüscher A., Finn J.A., Connolly J., Sebastià M.T., Collins R., Fothergill M., Porqueddu C., Brophy C., Huguenin-Elie O., Kirwan L., Nyfeler D. and Helgadóttir Á. (2008) Benefits of sward diversity for agricultural grasslands. Biodiversity 9, 29-32. Lüscher A., Soussana, J.F. and Huguenin-Elie O. (2011) Role and impacts of legumes in grasslands for high productivity and N gain from symbiotic N2 fixation. In: Lemaire G., Hodgson J. and Chabbi A. (eds) Grassland
Productivity and Ecosystem Services, CAB International, Wallingford, UK, pp. 101-107. Maizels R.M. and Yazdanbakhsh M. (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733-744. Marquard E., Weigelt A., Temperton V.M., Roscher C., Schumacher J., Buchmann N., Fischer M., Weisser W.W. and Schmid B. (2009) Plant species richness and functional composition drive overyielding in a six-year grassland experiment. Ecology 90, 3290-3302. McCaughey W.P., Wittenberg K. and Corrigan D. (1999) Impact of pasture type on methane production by lactating beef cows. Canadian Journal of Animal Science 79, 221-226. McMahon L.R., McAllister T.A., Berg B.P., Majak W., Acharya S.N., Popp J.D., Coulman B.E., Wang Y. and Cheng K.J. (2000) A review of the effect of forage condensed tannins on ruminal fermentation and bloat in grazing cattle. Canadian Journal of Plant Science 80, 469-485. Miller L.A., Moorby J.M., Davis D.R., Humphreys M.O., Scollan N.D., MacRae J.C. and Theodorou M.K. (2001) Increased concentration of water-soluble carbohydrate in perennial ryegrass (Lolium perenne L.): milk production from late-lactation dairy cows. Grass and Forage Science 56, 383-394. Min B.R., Barry T.N., Attwood G.T. and McNabb W.C. (2003) The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Animal Feed Science and Technology 106, 3-19. Mitchell K.J. (1956) Growth of pasture species under controlled environment. I. Growth at various levels of constant temperature. New Zealand Journal of Science and Technology 38A, 203-216. Molan A.L., Meagher L.P., Spencer P.A. and Sivakumaran S. (2003) Effect of flavan-3-ols on in vitro egg hatching, larval development and viability of infective larvae of Trichostrongylus colubriformis. International
Journal for Parasitology 33, 1691-1698. Molento M.B. (2009) Parasite control in the age of drug resistance and changing agricultural practices. Veterinary Parasitology 163, 229-234.
The Role of Grasslands in a Green Future 25
Mommer L., van Ruijven J., de Caluwe H., Smit-Tiekstra A.E., Wagemaker C.A.M., Ouborg N.J., Bögemann
G.M., van der Weerden G.M., Berendse F. and de Kroon H. (2010) Unveiling below-ground species abundance
in a biodiversity experiment: a test of vertical niche differentiation among grassland species. Journal of Ecology
98, 1117-1127.
Morin C., Bélanger G., Tremblay G.F., Bertrand A., Castonguay Y., Drapeau R., Michaud R., Berthiaume R.
and Allard G. (2011) Diurnal variations of nonstructural carbohydrates and nutritive value in alfalfa. Crop
Science 51, 1297-1306.
Mortensen M.C., Schuman G.E. and Ingram L.J. (2004) Carbon sequestration in rangelands interseeded with
Temperton V.M., Weigelt A., Weisser W.W. and Wilcke W. (2011) Plant diversity effects on aboveground and
belowground N pools in temperate grassland ecosystems: Development in the first 5 years after establishment.
Global Biogeochemical Cycles 25, GB2014, doi:10.1029/2010GB003869.
Orr R.J., Parson A.J., Penning P.D. and Treacher T.T. (1990) Sward composition, animal performance and the
potential production of grass/white clover swards continuously stocked with sheep. Grass and Forage Science
45, 325-336.
Palmborg C., Scherer-Lorenzen M., Jumpponen A., Carlsson G., Huss-Danell K. and Högberg P. (2005)
Inorganic soil nitrogen under grassland plant communities of different species composition and diversity. Oikos
110, 271-282.
Pelletier S., Tremblay G.F., Bélanger G., Bertrand A., Castonguay Y., Pageau D. and Drapeau R. (2010) Forage
nonstructural carbohydrates and nutritive value as affected by time of cutting and species. Agronomy Journal 102,
1388-1398.
Pellikaan W.F., Stringano E., Leenaars J., Bongers D.J.G.M., van Laar-van Schuppen S., Plant J. and Mueller-
Harvey I. (2011) Evaluating the effects of tannins on the extent and rate of in vitro measured gas and methane
production using the Automated Pressure Evaluation System (APES). Animal Feed Science and Technology 166-
167, 377-390.
Peyraud J.L. (1993) Comparaison de la digestion du trèfle blanc et des graminées prairiales chez la vache
laitière. Fourrages 135, 465-473.
Peyraud J.L., Le Gall A. and Lüscher A. (2009) Potential food production from forage legume-based-systems in
Europe: an overview. Irish Journal of Agricultural and Food Research 48, 115-135.
Peyraud J.L., Delaby L., Dourmad J.Y., Faverdin P., Morvan T. and Vertes F. (2012) Les systèmes de
polyculture-élevage pour bien valoriser l’azote. Innovations Agronomiques 22, 45-69.
Pflimlin A., Arnaud J.D., Gautier D. and Le Gall A. (2003) Les légumineuses fourragères, une voie pour
concilier autonomie en protéines et préservation de l’environnement. Fourrages 174, 183-203.
Phillips C.J.C. and James N.L. (1998) The effects of including white clover in perennial ryegrass pastures and
the height of mixed swards on the milk production, pasture selection and ingestive behaviour of dairy cows.
Animal Science 67, 195-202.
Piano E. and Pecetti L. (2010) Minor Legume Species. In: Boller B., Posselt U.K. and Veronesi F. (eds) Fodder
Crops and Amenity Grasses, Handbook of plant breeding, Vol. 5. Springer, New York, USA, pp. 477-500.
26 Grassland Science in Europe, Vol. 18
Pirhofer-Walzl K., Rasmussen J., Høgh-Jensen H., Eriksen J., Søegaard K. and Rasmussen J. (2012) Nitrogen transfer from forage legumes to nine neighbouring plants in a multi-species grassland. Plant and Soil 350, 71-84. Provenza F.D. and Villalba J.J. (2010) The role of natural plant products in modulating the immune system: an adaptable approach for combating disease in grazing animals. Small Ruminant Research 89, 131-139. Rasmussen J., Søegaard K., Pirhofer-Walzl K. and Eriksen J. (2012) N2-fixation and residual N effect of four legume species and four companion grass species. European Journal of Agronomy 36, 66-74. Ribeiro-Filho H.M.N., Delagarde R. and Peyraud J.L. (2003) Inclusion of white clover in strip-grazed perennial ryegrass swards: herbage intake and milk yield of dairy cows at different ages of sward regrowth. Animal
Science 77, 499-510. Ribeiro-Filho H.M.N., Delagarde R. and Peyraud, J.L. (2005) Herbage intake and milk yield of dairy cows grazing perennial ryegrass swards or white-clover/perennial rye grass swards at low- and medium-herbage allowances. Animal Feed Science and Technology 119, 13-27. Rochette P. and Janzen H.H. (2005) Towards a revised coefficient for estimating N2O emissions from legumes. Nutrient Cycling in Agroecosystems 73, 171-179. Rochon J.J., Doyle C.J., Greef J.M., Hopkins A., Molle G., Sitzia M., Scholefield D. and Smith C.J. (2004) Grazing legumes in Europe: a review of their status, management, benefits, research needs and future prospects. Grass and Forage Science 59, 197-214. Rockström J., Steffen W., Noone K., Persson Å., Chapin F.S., Lambin E.F., Lenton T.M., Scheffer M., Folke C., Schellnhuber H.J., Nykvist B., de Wit C.A., Hughes T., van der Leeuw S., Rodhe H., Sörlin S., Snyder P.K., Costanza R., Svedin U., Falkenmark M., Karlberg L., Corell R.W., Fabry V.J., Hansen J., Walker B., Liverman D., Richardson K., Crutzen P. and Foley J.A. (2009). A safe operating space for humanity. Nature 461, 472-475. Roscher C., Temperton V.M., Scherer-Lorenzen M., Schmitz M., Schumacher J., Schmid B., Buchmann N., Weisser W.W. and Schulze E.D. (2005) Overyielding in experimental grassland communities – irrespective of species pool or spatial scale. Ecology Letters 8, 419-429. Roscher C., Thein S., Schmid B. and Scherer-Lorenzen M. (2008) Complementary nitrogen use among potentially dominant species in a biodiversity experiment varies between two years. Journal of Ecology 96, 477-488. Roscher C., Thein S., Weigelt A., Temperton V.M., Buchmann N. and Schulze E.D. (2011) N2 fixation and performance of 12 legume species in a 6-year grassland biodiversity experiment. Plant and Soil 341, 333-348. Roughley R.J. and Dart P.J. (1970) Growth of Trifolium subterraneum L. selected for sparse and abundant nodulation as affected by root temperature and Rhizobium strain. Journal of Experimental Botany, 21, 776-786. Rouillé B., Lamy J.M. and Brunschwig P. (2010) Trois formes de consommation de la luzerne pour les vaches laitières. Rencontres Recherches Ruminants 17, 329. Russelle M.P., Lamb J.F.S., Montgomery B.R., Elsenheimer D.W., Miller B.S. and Vance C.P. (2001). Alfalfa rapidly remediates excess inorganic nitrogen at a fertilizer spill site. Journal of Environmental Quality 30, 30-36. Ruz-Jerez B.E., White R.E. and Ball P.R. (1994) Long-term measurement of denitrification in three contrasting pastures grazed by sheep. Soil Biology and Biochemistry 26, 29-39. Saratsis A., Regos I., Tzanidakis N., Voutzourakis N., Stefanakis A., Treuter D., Joachim A. and Sotiraki S. (2012) In vivo and in vitro efficacy of sainfoin (Onobrychis viciifolia) against Eimeria spp. in lambs. Veterinary
Parasitology 188, 1-9. Scherer-Lorenzen M., Palmborg C., Prinz A. and Schulze E.D. (2003) The role of plant diversity and composition for nitrate leaching in grasslands. Ecology 84, 1539-1552. Schils R.L.M. (1994) Nitrate losses from grazed grass and grass/clover pastures on clay soil. Meststoffen 1994, 78-84. Schils R.L.M., Verhagen A., Aarts H.F.M. and Šebek, L.B.J. (2005) A farm level approach to define successful mitigation strategies for GHG emissions from ruminant livestock systems. Nutrient Cycling in Agroecosystems 71, 163-175. Schmid B., Hector A., Saha P. and Loreau M. (2008) Biodiversity effects and transgressive overyielding. Journal of Plant Ecology 1, 95-102. Scholefield D., Lockyer D.R., Whitehead D.C. and Tyson K.C. (1991) A model to predict transformations and losses of nitrogen in UK pastures grazed by beef cattle. Plant and Soil 132, 165-177. Schulze E., Luyssaert S., Ciais P., Freibauer A., Janssens I.A., Soussana J.F., Smith P., Grace J., Levin I., Thiruchittampalam B., Heimann M., Dolman A.J., Valentini R., Bousquet P., Peylin P., Peters W., Rödenbeck C., Etiope G., Vuichard N., Wattenbach M., Nabuurs G.J., Poussi Z., Nieschulze J. and Gash J.H. (2009) Importance of methane and nitrous oxide for Europe's terrestrial greenhouse-gas balance. Nature Geoscience 2, 842-850. Schwank O., Blum H. and Nösberger J. (1986) The influence of irradiance distribution on the growth of white clover (Trifolium repens L.) in differently managed canopies of permanent grassland. Annals of Botany 57, 273-281.
The Role of Grasslands in a Green Future 27
Scioneaux A.N, Schmidt M.A., Moore M.A., Lindroth R.L., Wooley S.C. and Hagerman A.E. (2011) Qualitative variation in proanthocyanidin composition of Populus species and hybrids: genetics is the key. Journal of
Chemical Ecology 37, 57-70. Sergeeva A.G. (1955) The effect of lucerne and sainfoin on the water-stable structure of soils under irrigation.
Pocvovedenie 12, 35-42. Sölter U., Hopkins A., Sitzia M., Goby J.P. and Greef J.M. (2007) Seasonal changes in herbage mass and nutritive value of a range of grazed legume swards under Mediterranean and cool temperate conditions. Grass
and Forage Science 62, 372-388. Soussana J.F. and Hartwig U.A. (1996) The effects of elevated CO2 on symbiotic N2 fixation: a link between the carbon and nitrogen cycles in grassland ecosystems. Plant and Soil 187, 321-332. Soussana J.F. and Lüscher A. (2007) Temperate grasslands and global atmospheric change: a review. Grass and
Forage Science 62, 127-134. Soussana J.F. and Tallec T. (2010) Can we understand and predict the regulation of biological N2 fixation in grassland ecosystems? Nutrient Cycling in Agroecosystems 88, 197-213. Soussana J.F., Minchin F.R., Macduff J.H., Raistrick N., Abberton M.T., and Michaelson-Yeates T.P.T. (2002) A simple model of feedback regulation for nitrate uptake and N2 fixation in contrasting phenotypes of white clover. Annals of Botany 90, 139-147. Soussana J.F., Loiseau P., Vuichard N., Ceschia E., Balesdent J., Chevallier T. and Arrouays D. (2004) Carbon cycling and sequestration opportunities in temperate grasslands. Soil Use and Management 20, 219-230. Soussana J.F., Tallec T. and Blanfort V. (2010) Mitigating the greenhouse gas balance of ruminant production systems through carbon sequestration in grasslands. Animal 4, 334-350. Sparrow S. D., Cochran V. L. and Sparrow E. B. (1995) Dinitrogen fixation by seven legume crops in Alaska. Agronomy Journal 87, 34-41. Spehn E.M., Scherer-Lorenzen M., Schmid B., Hector A., Caldeira M.C., Dimitrakopoulos P.G., Finn J.A., Jumpponen A., O'Donnovan G., Pereira J.S., Schulze E.D., Troumbis A.Y. and Körner C. (2002) The role of legumes as a component of biodiversity in a cross-European study of grassland biomass nitrogen. Oikos 98, 205-218. Speijers M.H.M., Fraser M.D., Theobald V.J. and Haresign W. (2004) The effects of grazing forage legumes on the performance of finishing lambs. The Journal of Agricultural Science 142, 483-493. Steg A., Van Straalen W.M., Hindle V.A., Wensink W.A., Dooper F.M.H. and Schils R.L.M. (1994) Rumen degradation and intestinal digestion of grass and clover at two maturity levels during the season in dairy cows. Grass and Forage Science 49, 378-390. Stoate C., Báldi A., Beja P., Boatman N.D., Herzon I., van Doorn A., de Snoo G.R., Rakosy L. and Ramwell C. (2009) Ecological impacts of early 21st century agricultural change in Europe – A review. Journal of
Environmental Management 91, 22-46. Stringano E., Hayot Carbonero C., Smith L.M.J., Brown R.H. and Mueller-Harvey I. (2012) Proanthocyanidin diversity in the EU ‘HealthyHay’ sainfoin (Onobrychis viciifolia) germplasm collection. Phytochemistry 77, 197-208. Sturludóttir E., Brophy C., Bélanger G., Gustavsson A.M., Jørgensen M., Lunnan T. and Helgadóttir Á. (2013) Benefits of mixing grasses and legumes for herbage yield and nutritive value in Northern Europe and Canada. Grass and Forage Science doi: 10.1111/gfs.12037. Suter D., Briner H.U. and Lüscher A. (2007) Effect of Lolium perenne L. variety on the botanical composition of grass-clover mixtures. Grassland Science in Europe 12, 417-420. Suter D., Huguenin-Elie O., Nyfeler D. and Lüscher A. (2010) Agronomically improved grass-legume mixtures: higher dry matter yields and more persistent legume proportions. Grassland Science in Europe 15, 761-763. Suter D., Rosenberg E., Mosimann E. and Frick R. (2012) Standardmischungen für den Futterbau: Revision 2013-2016. Agrarforschung Schweiz 3, 1-12. Tallec T., Diquélou S., Avice J.C., Lesuffleur F., Lemauviel-Lavenant S., Cliquet J.B. and Ourry A. (2009) Availability of N and S affect nutrient acquisition efficiencies differently by Trifolium repens and Lolium
perenne when grown in monoculture or in mixture. Environmental and Experimental Botany 66, 309-316. Tamminga S., Bannink A., Dijkstra J. and Zom R. (2007) Feeding strategies to reduce methane loss in cattle. Animal Science Group, Wageningen University, February 2007, Report 34, 44p. Available at: http://www2.asg.wur.nl/NR/rdonlyres/F81D8745-6596-4296-A292-8553950E2B98/42707/34.pdf (accessed on 6 February 2013). Tavendale M.H., Meagher L.P., Pacheco D., Walker N., Attwood G.T. and Sivakumaran S. (2005) Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Animal Feed Science and Technology 123-124, 403-419.
28 Grassland Science in Europe, Vol. 18
Temperton V.M., Mwangi P.N., Scherer-Lorenzen M., Schmid B. and Buchmann N. (2007) Positive interactions
between nitrogen-fixing legumes and four different neighbouring species in a biodiversity experiment.
Oecologia 151, 190-205.
Theodoridou K., Aufrère J., Andueza D., Le Morvan A., Picard F., Stringano E., Pourrat J., Mueller-Harvey I.,
and Baumont R. (2011) Effect of plant development during first and second growth cycle on chemical
composition, condensed tannins and nutritive value of three sainfoin (Onobrychis viciifolia) varieties and
lucerne. Grass and Forage Science 66, 402-414.
Thomas R.J. (1992) The role of the legume in the nitrogen cycle of productive and sustainable pastures. Grass
and Forage Science 47, 133-142.
Thornton P.K. (2010) Livestock production: recent trends, future prospects. Philosophical Transactions of the
Royal Society B: Biological Sciences 365, 2853-2867.
Tibe O., Pernthaner A., Sutherland I., Lesperance L. and Harding D.R.K. (2012) Condensed tannins from
Botswanan forage plants are effective priming agents of T cells in ruminants. Veterinary Immunology and
Immunopathology 146, 237-244.
Tilman D. (1999) The ecological consequences of changes in biodiversity: A search for general principles.
Ecology 80, 1455-1474.
Tremblay G.F., Berthiaume R., Bélanger G., Bertrand A., Castonguay Y., Michaud R., Pelletier S., Brito A.,
Lafrenière C., Drapeau R. and Allard G. (2011) Nonstructural carbohydrates: How to increase their
concentration in forages and how does it affect animal performance? In: Proceedings of the 47th
Eastern
Nutrition Conference, Montreal, Quebec, CA, pp. 219-243. Trenbath B.R. (1974) Biomass productivity of mixtures. Advances in Agronomy 26, 177-210.
Ulyatt M.J. (1970) Evaluation of pasture quality under New Zealand conditions. Proceedings of the New Zealand
Grassland Association, 32, 61-68.
Undersander D., McCalsin M., Shaeffer C., Whalen D., Miller D., Putnam D. and Orloff S. (2009) Low lignin
alfalfa: Redefining the yield/quality tradeoff. Available at: http://alfalfa.ucdavis.edu/+symposium/2009/
(accessed on 6 February 2013).
Unkovich M.J., Baldock J. and Peoples M.B. (2010) Prospects and problems of simple linear models for
estimating symbiotic N2 fixation by crop and pasture legumes. Plant and Soil 329, 75-89.
Van Dorland H.A., Wettstein H.R., Leuenberger H. and Kreuzer M. (2007) Effect of supplementation of fresh
and ensiled clovers to ryegrass on nitrogen loss and methane emissions in dairy cows. Livestock Science 111, 57-
69.
Van Ruijven J. and Berendse F. (2003) Positive effects of plant species diversity on productivity in the absence
of legumes. Ecology Letters 6, 170-175.
Veronesi F., Brummer E.C. and Huyghe C. (2010) Alfalfa. In: Boller B., Posselt U.K. and Veronesi F. (eds)
Fodder Crops and Amenity Grasses, Handbook of plant breeding, Vol. 5. Springer, New York, USA, pp. 395-
438.
Vertès F., Simon J.C., Le Corre L. and Decau M.L. (1997) Nitrogen flows in grazed pastures. II. Study of flows
and their effects on leaching. Fourrages 151, 263-280.
Vörösmarty C.J., McIntyre P.B., Gessner M.O., Dudgeon D., Prusevich A., Green P., Glidden S., Bunn S.E.,
Sullivan C.A., Reidy Liermann C. and Davies P.M. (2010) Global threats to human water security and river
biodiversity. Nature 467, 555-561.
Waghorn G.C. (2008) Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and
goat production – Progress and challenges. Animal Feed Science and Technology 147, 116-139.
Waghorn G.C. and Hegarty R.S. (2011) Lowering ruminant methane emissions through improved feed
conversion efficiency. Animal Feed Science and Technology 166-167, 291-301.
Waghorn G.C., Shelton I.D. and Thomas V.J. (1989) Particle breakdown and rumen digestion of fresh ryegrass
(Lolium perenne L.) and lucerne (Medicago sativa L.) fed to cows during a restricted feeding period. British
Journal of Nutrition 61, 409-423.
Waghorn G.C., Douglas G.B., Niezen J.H., McNabb W.C. and Foote A.G. (1998) Forages with condensed
tannins – their management and nutritive value for ruminants. Proceedings of the New Zealand Grassland
Association 60, 89-98.
Waghorn G.C., Woodward S.L., Tavendale M. and Clark D.A. (2006) Inconsistencies in rumen methane
production – effects of forage composition and animal genotype. International Congress Series 1293, 115-118.
Wang Y., Barbieri L.R., Berg B.P. and McAllister T.A. (2007) Effects of mixing sainfoin with alfalfa on
ensiling, ruminal fermentation and total tract digestion of silage. Animal Feed Science and Technology 135, 296-
314.
Wang Y., Majak W. and McAllister T.A. (2012) Frothy bloat in ruminants: cause, occurrence, and mitigation
strategies. Animal Feed Science and Technology 172, 103-114.
The Role of Grasslands in a Green Future 29
Weightman R.M., Cottrill B.R., Wiltshire J.J.J., Kindred D.R. and Sylvester-Bradley R. (2011) Opportunities for
avoidance of land-use change through substitution of soya bean meal and cereals in European livestock diets
with bioethanol coproducts. Global Change Biology Bioenergy 3, 158-170.
Weiss P. and Raymond F. (1993) L’ensilage de trèfle violet pour l’engraissement des taurillons. Fourrages 134,
283-286.
Wilkins R.J., Gibb M.J., Huckle C.A. and Clements A.J. (1994) Effect of supplementation on production by
spring-calving dairy cows grazing swards of differing clover content. Grass and Forage Science, 49, 465-475.
Woledge J. (1988) Competition between grass and clover in spring as affected by nitrogen-fertiliser. Annals of
Applied Biology 112, 175-186.
Woodward S.L., Waghorn G.C., Lassey K.R. and Laboyrie P.G. (2002) Does feeding sulla (Hedysarum
coronarium) reduce methane emissions from dairy cows? Proceedings of New Zealand Society of Animal
Production 62, 227-230.
Woodward S.L., Waghorn G.C. and Laboyrie P.G. (2004) Condensed tannins in birdsfoot trefoil (Lotus
corniculatus) reduce methane emissions from dairy cows. Proceedings of New Zealand Society of Animal
Production 64, 160-164.
Woodward S.L., Waghorn G.C., Watkins K.A. and Bryant M.A. (2009) Feeding birdsfoot trefoil (Lotus
corniculatus) reduces the environmental impacts of dairy farming. Proceeding of the New Zealand Society of
Animal Production 69, 179-183.
Yachi S. and Loreau M. (1999) Biodiversity and ecosystem productivity in a fluctuating environment: The
insurance hypothesis. Proceedings of the National Academy of Sciences of the United States of America 96, 1463-1468.
Zanetti S., Hartwig U.A., van Kessel C., Lüscher A., Hebeisen T., Frehner M., Fischer B.U., Hendrey G.R.,
Blum H. and Nösberger J. (1997) Does nitrogen nutrition restrict the CO2 response of fertile grassland lacking